Three consecutive generations of nephridia occur during development of Platynereis dumerilii (Annelida, Polychaeta)

Morphology and Evolution of Animals, Philipps-Universität Marburg, Karl-von-Frisch-Strasse 8, Marburg, Germany.
Developmental Dynamics (Impact Factor: 2.38). 07/2010; 239(7):1967-76. DOI: 10.1002/dvdy.22331
Source: PubMed


Molecular data for nephridial development in polychaetes are not available yet. The scope of our work was to establish a reference system for future investigations using two markers for nephridial development: beta-tubulin as marker for cilia and alkaline phosphatase (AP) activity for secretory epithelia. The markers identified, unexpectedly, three consecutively forming generations of nephridia: (1) a transitory unciliated, but AP-positive head kidney, (2) a transitory larval nephridium, which undergoes a morphological transition from a protonephridium to a funnelled nephridium concomitant with the development of the coelomic cavity and finally, (3) the serially arranged metanephridia. The spatial arrangement of larval and definitive nephridia, revealed an up to now unknown developmental boundary between the synchronously forming larval and the serially proliferating definitive segments. Development of three consecutive sets of nephridia with different morphology and biochemical properties was unexpected and reveals an interesting multistep process in the development of excretory structures in Platynereis.

Download full-text


Available from: Monika Hassel, Sep 18, 2014
1 Follower
41 Reads
  • Source
    • "In addition, two small Pdu-twist expressing patches can be observed on both sides of the 24 hpf larva (Fig. 2 (a, a′, arrows)). According to their location in the episphere, it is most convincing that these cells refer to the transitory larval head kidneys (Hasse et al. 2010). During further development, Pdu-twist-positive cells of the three bilateral domains expand around the ventral and dorsal chaetal sacs and give rise to the trunk musculature (Fig. 2 (c–i)), while the stomodeal expression increases in intensity and labels the developing pharyngeal muscles (Fig. 2 (c, e, arrowheads , i, g)). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The basic helix-loop-helix transcription factor twist plays a key role during mesoderm development in Bilateria. In this study, we identified a twist ortholog in the polychaete annelid Platynereis dumerilii and analyze its expression during larval development, postlarval growth up to the adult stage, and caudal regeneration after amputation of posterior segments. At late larval stages, Pdu-twist is expressed in the mesodermal anlagen and in developing muscles. During adulthood and caudal regeneration, Pdu-twist is expressed in the posterior growth zone, in mesodermal cells within the newly forming segments and budding parapodia. Our results indicate that Pdu-twist is involved in mesoderm formation during larval development, posterior growth, and caudal regeneration.
    Development Genes and Evolution 09/2013; 223(5):319-28. DOI:10.1007/s00427-013-0448-6 · 2.44 Impact Factor
  • Source
    • "In addition, both types do occur subsequently during ontogeny in certain polychaetes (e.g. [42]). The finding of a cilium in a podocyte of Lepidochitona corrugata – remarkably the first report of a podocyte bearing a cilium in a mollusc – lends substantial support to this concept. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Background Two types of excretory systems, protonephridia and metanephridial systems are common among bilaterians. The homology of protonephridia of lophotrochozoan taxa has been widely accepted. In contrast, the homology of metanephridial systems – including coelomic cavities as functional units – among taxa as well as the homology between the two excretory systems is a matter of ongoing discussion. This particularly concerns the molluscan kidneys, which are mostly regarded as being derived convergently to the metanephridia of e.g. annelids because of different ontogenetic origin. A reinvestigation of nephrogenesis in polyplacophorans, which carry many primitive traits within molluscs, could shed light on these questions. Results The metanephridial system of Lepidochitona corrugata develops rapidly in the early juvenile phase. It is formed from a coelomic anlage that soon achieves endothelial organization. The pericardium and heart are formed from the central portion of the anlage. The nephridial components are formed by outgrowth from lateral differentiations of the anlage. Simultaneously with formation of the heart, podocytes appear in the atrial wall of the pericardium. In addition, renopericardial ducts, kidneys and efferent nephroducts, all showing downstream ciliation towards the internal lumen, become differentiated (specimen length: 0.62 mm). Further development consists of elongation of the kidney and reinforcement of filtration and reabsorptive structures. Conclusions During development and in fully formed condition the metanephridial system of Lepidochitona corrugata shares many detailed traits (cellular and overall organization) with the protonephridia of the same species. Accordingly, we suggest a serial homology of various cell types and between the two excretory systems and the organs as a whole. The formation of the metanephridial system varies significantly within Mollusca, thus the mode of formation cannot be used as a homology criterion. Because of similarities in overall organization, we conclude that the molluscan metanephridial system is homologous with that of the annelids not only at the cellular but also at the organ level.
    Frontiers in Zoology 09/2012; 9(1):23. DOI:10.1186/1742-9994-9-23 · 3.05 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Alkaline phosphatase enzymes are found throughout the living world and fulfil a variety of functions. They have been linked to regeneration, stem cells and biomineralisation in a range of animals. Here we describe the pattern of alkaline phosphatase activity in a spiralian appendage, the operculum of the serpulid polychaete Pomatoceros lamarckii. The P. lamarckii operculum is reinforced by a calcified opercular plate and is capable of rapid regeneration, making it an ideal model system to study these key processes in annelids. Alkaline phosphatase activity is present in mesodermal tissues of both intact and regenerating opercular filaments, in a strongly regionalised pattern correlated with major morphological features. Based on the lack of epidermal activity and the broad distribution of staining in mesodermal tissues, calcification- or stem cell-specific roles are unlikely. Transcriptomic data reveal that at least four distinct genes contribute to the detected activity. Opercular alkaline phosphatase activity is sensitive to levamisole. Phylogenetic analysis of metazoan alkaline phosphatases indicates homology of the P. lamarckii sequences to other annelid alkaline phosphatases, and shows that metazoan alkaline phosphatase evolution was characterised by extensive lineage-specific duplications.
    The International Journal of Developmental Biology 01/2014; 58(6-7-8):635-642. DOI:10.1387/ijdb.140116df · 1.90 Impact Factor